journal article·2022-09-28Open access

Construction of Artificial Ovaries with Decellularized Porcine Scaffold and Its Elicited Immune Response after Xenotransplantation in Mice

Tong Wu, Yue-Yue Gao, Xia-Nan Tang, Jin-Jin Zhang, Shi-Xuan Wang

Abstract

Substitution by artificial ovary is a promising approach to restore ovarian function, and a decellularized extracellular matrix can be used as a supporting scaffold. However, biomimetic ovary fabrication and immunogenicity requires more investigation. In this study, we proposed an effective decellularization protocol to prepare ovarian scaffolds, which were characterized by few nuclear substances and which retained the extracellular matrix proteins. The ovarian tissue shape and 3-dimensional structure were well-preserved after decellularization. Electron micrographs demonstrated that the extracellular matrix fibers in the decellularized group had similar porosity and structure to those of native ovaries. Semi-quantification analysis confirmed that the amount of extracellular matrix proteins was reduced, but the collagen fiber length, width, and straightness did not change significantly. Granulosa cells were attached and penetrated into the decellularized scaffold and exhibited high proliferative activity with no visible apoptotic cells on day 15. Follicle growth was compromised on day 7. The implanted artificial ovaries did not restore endocrine function in ovariectomized mice. The grafts were infiltrated with immune cells within 3 days, which damaged the artificial ovary morphology. The findings suggest that immune rejection plays an important role when using artificial ovaries.
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Research context

OpenAlex topics: Tissue Engineering and Regenerative Medicine · Electrospun Nanofibers in Biomedical Applications · Additive Manufacturing and 3D Printing Technologies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

National Clinical Research Center for Obstetrical and Gynecological Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China

Key Laboratory of Cancer Invasion and Metastasis, Ministry of Education, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China

Department of Obstetrics and Gynecology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China

Funding

National Natural Science Foundation of China

References (47)

Show source-provided references
1. Developmental Programming of Ovarian Functions and Dysfunctions10.1016/bs.vh.2018.01.017 ↗
2. Agarwal, S., Alzahrani, F.A., and Ahmed, A. (2018). Hormone Replacement Therapy: Would it be Possible to Replicate a Functional Ovary?. Int. J. Mol. Sci., 19.10.3390/ijms19103160 ↗
3. Three-dimensional bioprinting of artificial ovaries by an extrusion-based method using gelatin-methacryloyl bioink10.1080/13697137.2021.1921726 ↗
4. The artificial ovary: Current status and future perspectives10.2217/fon-2016-0202 ↗
5. Porzionato, A., Stocco, E., Barbon, S., Grandi, F., Macchi, V., and De Caro, R. (2018). Tissue-Engineered Grafts from Human Decellularized Extracellular Matrices: A Systematic Review and Future Perspectives. Int. J. Mol. Sci., 19.10.3390/ijms19124117 ↗
6. Lamellar Keratoplasty Treatment of Fungal Corneal Ulcers With Acellular Porcine Corneal Stroma10.1111/ajt.13096 ↗
7. Natural Sources of Extracellular Matrix for Cardiac Repair10.1007/978-3-319-97421-7_6 ↗
8. Production and transplantation of bioengineered lung into a large-animal model10.1126/scitranslmed.aao3926 ↗
9. Initiation of puberty in mice following decellularized ovary transplant10.1016/j.biomaterials.2015.01.051 ↗
10. Decellularization of the mouse ovary: Comparison of different scaffold generation protocols for future ovarian bioengineering10.1186/s13048-019-0531-3 ↗
11. Whole-ovary decellularization generates an effective 3D bioscaffold for ovarian bioengineering10.1007/s10815-020-01784-9 ↗
12. Evaluating two ovarian decellularization methods in three species10.1016/j.msec.2019.04.092 ↗
13. Optimizing the Cell Seeding Protocol to Human Decellularized Ovarian Scaffold: Application of Dynamic System for Bio-Engineering
14. Creation of a Bioengineered Ovary: Isolation of Female Germline Stem Cells for the Repopulation of a Decellularized Ovarian Bioscaffold10.1007/978-1-0716-1246-0_9 ↗
15. Ovarian extracellular matrix-based hydrogel for human ovarian follicle survival in vivo: A pilot work10.1002/jbm.b.34974 ↗
16. Initial steps in reconstruction of the human ovary: Survival of pre-antral stage follicles in a decellularized human ovarian scaffold10.1093/humrep/dez077 ↗
17. Large animal models for the study of ovarian follicular dynamics in women10.1016/j.theriogenology.2012.04.010 ↗
18. Decellularized scaffolds in regenerative medicine10.18632/oncotarget.10945 ↗
19. Pennarossa, G., De Iorio, T., Gandolfi, F., and Brevini, T.A.L. (2021). Ovarian Decellularized Bioscaffolds Provide an Optimal Microenvironment for Cell Growth and Differentiation In Vitro. Cells, 10.10.3390/cells10082126 ↗
20. The decellularized ovary as a potential scaffold for maturation of preantral ovarian follicles of prepubertal mice10.1080/19396368.2021.1968542 ↗
21. Co-culture with peritoneum mesothelial stem cells supports the in vitro growth of mouse ovarian follicles10.1002/jbm.a.37260 ↗
22. Fertility preservation in women with cancer10.1016/S0140-6736(14)60834-5 ↗
23. Decellularized Cartilage Matrix as a Novel Biomatrix for Cartilage Tissue-Engineering Applications10.1089/ten.tea.2011.0705 ↗
24. Effects of freezing/thawing on the mechanical properties of decellularized lungs10.1002/jbm.a.34708 ↗
25. The mechanism of detergent solubilization of lipid bilayers10.1016/j.bpj.2013.06.007 ↗
26. Characteristics of a decellularized human ovarian tissue created by combined protocols and its interaction with human endometrial mesenchymal cells10.1007/s40204-021-00163-6 ↗
27. Tissue Engineered Human Amniotic Membrane Application in Mouse Ovarian Follicular Culture10.1007/s10439-017-1836-2 ↗
28. Fluorescence of Picrosirius Red Multiplexed with Immunohistochemistry for the Quantitative Assessment of Collagen in Tissue Sections10.1369/0022155417718541 ↗
29. Determination of collagen content within picrosirius red stained paraffin-embedded tissue sections using fluorescence microscopy10.1016/j.mex.2015.02.007 ↗
30. Effects of Alginate Concentration and Ovarian Cells on In Vitro Development of Mouse Preantral Follicles: A Factorial Study
31. Embryonic Fibroblasts Enable the Culture of Primary Ovarian Follicles within Alginate Hydrogels10.1089/ten.tea.2011.0418 ↗
32. The stage-dependent inhibitory effect of porcine follicular cells on the development of preantral follicles10.1016/S0378-4320(02)00119-7 ↗
33. Bioengineering the Ovarian Follicle Microenvironment10.1146/annurev-bioeng-071813-105131 ↗
34. Growth In Vitro of Granulosa Cell–Oocyte Complexes of the Mouse10.1007/978-1-4939-8603-3_1 ↗
35. A Revised Protocol for In Vitro Development of Mouse Oocytes from Primordial Follicles Dramatically Improves Their Developmental Competence110.1095/biolreprod.102.013029 ↗
36. Xenogeneic Decellularized Scaffold: A Novel Platform for Ovary Regeneration10.1089/ten.tec.2016.0410 ↗
37. Decellularized scaffold and its elicited immune response towards the host: The underlying mechanism and means of immunomodulatory modification10.1039/D1BM00470K ↗
38. Immune response after allogeneic transplantation of decellularized uterine scaffolds in the rat10.1088/1748-605X/abfdfe ↗
39. Immune risk assessment of residual αGal in xenogeneic decellularized cornea using GTKO mice10.1093/rb/rbaa020 ↗
40. Combined blockade of complement C5 and TLR co-receptor CD14 synergistically inhibits pig-to-human corneal xenograft induced innate inflammatory responses10.1016/j.actbio.2021.03.047 ↗
41. Decellularized ECM-derived bioinks: Prospects for the future10.1016/j.ymeth.2019.04.019 ↗
42. The biocompatibility and immunogenicity study of decellularized tracheal matrix
43. In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation10.1016/j.biomaterials.2016.03.024 ↗
44. Preparation and evaluation of decellularized porcine carotid arteries cross-linked by genipin: The preliminary results10.1007/s10561-017-9675-9 ↗
45. Laronda, M.M., Rutz, A.L., Shah, R.N., and Woodruff, T.K. (2019). Artificial Ovary. (10479980), U.S. Patent.
46. Mouse ovarian follicle growth in an amniotic membrane-based hydrogel10.1177/08853282221094193 ↗
47. Decellularized human ovarian scaffold based on a sodium lauryl ester sulfate (SLES)-treated protocol, as a natural three-dimensional scaffold for construction of bioengineered ovaries10.1186/s13287-018-0971-5 ↗